The microbiome of potentially malignant oral leukoplakia exhibits enrichment for Fusobacterium, Leptotrichia, Campylobacter, and Rothia species

Frontiers in Microbiology

Volumn 8, Issue DEC, 2017, Pages

  Amer, Abdrazak ^a   Galvin, Sheila ^a   Healy, Claire M ^a   Moran, Gary P ^a  

^a DUBLIN DENTAL UNIVERSITY HOSPITAL   (Ireland)

Author keywords

Campylobacter; Fusobacteria; Microbiome; Oral cancer; Oral leukoplakia; Rothia mucilaginosa

Indexed keywords

RNA 16S;

ADULT; ARTICLE; BACTERIAL COLONIZATION; CAMPYLOBACTER; CAMPYLOBACTER CONCISUS; CANDIDA; CLINICAL ARTICLE; COLORECTAL CANCER; COMMUNITY STRUCTURE; CONTROLLED STUDY; DISEASE COURSE; DNA EXTRACTION; DNA SEQUENCE; DYSPLASIA; FIRMICUTES; FUSOBACTERIUM; HUMAN; HUMAN TISSUE; LEPTOTRICHIA; LEUKOPLAKIA; NONHUMAN; ORAL BIOPSY; REAL TIME POLYMERASE CHAIN REACTION; ROTHIA; ROTHIA MUCILAGINOSA; SEQUENCE ANALYSIS;

EID: 85036569936     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2017.02391     Document Type: Article

References (40)

1. Abdulrahim, M. H., McManus, B. A., Flint, S. R., and Coleman, D. C. (2013). Genotyping Candida albicans from Candida leukoplakia and non-Candida leukoplakia shows no enrichment of multilocus sequence typing clades but enrichment of ABC genotype C in Candida leukoplakia. PLOS ONE 8:e73738. doi: 10.1371/journal.pone.0073738
2. Abed, J., Emgård, J. E. M., Zamir, G., Faroja, M., Almogy, G., Grenov, A., et al. (2016). Fap2 mediates Fusobacterium nucleatum colorectal adenocarcinoma enrichment by binding to tumor-expressed Gal-GalNAc. Cell Host Microbe 20, 215-225. doi: 10.1016/j.chom.2016.07.006
3. Al-hebshi, N. N., Nasher, A. T., Maryoud, M. Y., Homeida, H. E., Chen, T., Idris, A. M., et al. (2017). Inflammatory bacteriome featuring Fusobacterium nucleatum and Pseudomonas aeruginosa identified in association with oral squamous cell carcinoma. Sci. Rep. 7:1834. doi: 10.1038/s41598-017-02079-3
4. Alnuaimi, A. D., Wiesenfeld, D., O'Brien-Simpson, N. M., Reynolds, E. C., and McCullough, M. J. (2015). Oral Candida colonization in oral cancer patients and its relationship with traditional risk factors of oral cancer: a matched case-control study. Oral Oncol. 51, 139-145. doi: 10.1016/j.oraloncology.2014.11.008
5. Binder Gallimidi, A., Fischman, S., Revach, B., Bulvik, R., Maliutina, A., Rubinstein, A. M., et al. (2015). Periodontal pathogens Porphyromonas gingivalis and Fusobacterium nucleatum promote tumor progression in an oral-specific chemical carcinogenesis model. Oncotarget 6, 22613-22623. doi: 10.18632/oncotarget.4209
6. Castellarin, M., Warren, R. L., Freeman, J. D., Dreolini, L., Krzywinski, M., Strauss, J., et al. (2011). Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res. 22, 299-306. doi: 10.1101/gr.126516.111
7. Diaz, P. I., Strausbaugh, L. D., and Dongari-Bagtzoglou, A. (2014). Fungal-bacterial interactions and their relevance to oral health: linking the clinic and the bench. Front. Cell Infect. Microbiol. 4:101. doi: 10.3389/fcimb.2014.00101
8. Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C., and Knight, R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194-2200. doi: 10.1093/bioinformatics/btr381
9. Frank, J. A., Reich, C. I., Sharma, S., Weisbaum, J. S., Wilson, B. A., and Olsen, G. J. (2008). Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl. Environ. Microbiol. 74, 2461-2470. doi: 10.1128/AEM.02272-07
10. Gillison, M. L., Koch, W. M., Capone, R. B., Spafford, M., Westra, W. H., Wu, L., et al. (2000). Evidence for a causal association between human papillomavirus and a subset of head and neck cancers. J. Natl. Cancer Inst. 92, 709-720. doi: 10.1093/jnci/92.9.709
11. Ho, M. W., Risk, J. M., Woolgar, J. A., Field, E. A., Field, J. K., Steele, J. C., et al. (2012). The clinical determinants of malignant transformation in oral epithelial dysplasia. Oral Oncol. 48, 969-976. doi: 10.1016/j.oraloncology.2012.04.002
12. Homann, N., Jousimies-Somer, H., Jokelainen, K., Heine, R., and Salaspuro, M. (1997). High acetaldehyde levels in saliva after ethanol consumption: methodological aspects and pathogenetic implications. Carcinogenesis 18, 1739-1743. doi: 10.1093/carcin/18.9.1739
13. Hu, X., Zhang, Q., Hua, H., and Chen, F. (2016). Changes in the salivary microbiota of oral leukoplakia and oral cancer. Oral Oncol. 56, e6-e8. doi: 10.1016/j.oraloncology.2016.03.007
14. Illumina (2013). 16S Metagenomic Sequencing Library Preparation, 1-28. Available at: http://support.illumina.com/documents/documentation/chemistry_documentation/16s/16s-metagenomic-library-prep-guide-15044223-b.pdf [accessed January 8, 2017]
15. Johnson, N. W., Jayasekara, P., and Amarasinghe, A. A. H. K. (2011). Squamous cell carcinoma and precursor lesions of the oral cavity: epidemiology and aetiology. Periodontol 2000 57, 19-37. doi: 10.1111/j.1600-0757.2011.00401.x
16. Kobayashi, T., Uchibori, S., Tsuzukibashi, O., Goto, H., and Aida, M. (2012). A selective medium for Rothia mucilaginosa and its distribution in oral cavities. J. Microbiol. Methods 91, 364-365. doi: 10.1016/j.mimet.2012.09.011
17. Kostic, A. D., Gevers, D., Pedamallu, C. S., Michaud, M., Duke, F., Earl, A. M., et al. (2011). Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res. 22, 292-298. doi: 10.1101/gr.126573.111
18. Kraneveld, E. A., Buijs, M. J., Bonder, M. J., Visser, M., Keijser, B. J. F., Crielaard, W., et al. (2012). The relation between oral Candida load and bacterial microbiome profiles in Dutch older adults. PLOS ONE 7:e42770. doi: 10.1371/journal.pone.0042770.s008
19. Liu, W., Shi, L.-J., Wu, L., Feng, J.-Q., Yang, X., Li, J., et al. (2012). Oral cancer development in patients with leukoplakia-clinicopathological factors affecting outcome. PLOS ONE 7:e34773. doi: 10.1371/journal.pone.0034773
20. Mager, D. L., Haffajee, A. D., Devlin, P. M., Norris, C. M., Posner, M. R., and Goodson, J. M. (2005). The salivary microbiota as a diagnostic indicator of oral cancer: a descriptive, non-randomized study of cancer-free and oral squamous cell carcinoma subjects. J. Transl. Med. 3:27. doi: 10.1186/1479-5876-3-27
21. Marttila, E., Uittamo, J., Rusanen, P., Lindqvist, C., Salaspuro, M., and Rautemaa, R. (2013). Acetaldehyde production and microbial colonization in oral squamous cell carcinoma and oral lichenoid disease. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. 116, 61-68. doi: 10.1016/j.oooo.2013.02.009
22. McCullough, M., Jaber, M., Barrett, A. W., Bain, L., Speight, P. M., and Porter, S. R. (2002). Oral yeast carriage correlates with presence of oral epithelial dysplasia. Oral Oncol. 38, 391-393. doi: 10.1016/S1368-8375(01)00079-3
23. Mills, A. L., and Alexander, M. (1976). N-Nitrosamine formation by cultures of several microorganisms. Appl. Environ. Microbiol. 31, 892-895
24. Moritani, K., Takeshita, T., Shibata, Y., Ninomiya, T., Kiyohara, Y., and Yamashita, Y. (2015). Acetaldehyde production by major oral microbes. Oral Dis. 21, 748-754. doi: 10.1111/odi.12341
25. Nagy, K. N., Sonkodi, I., Szöke, I., Nagy, E., and Newman, H. N. (1998). The microflora associated with human oral carcinomas. Oral Oncol. 34, 304-308. doi: 10.1016/S1368-8375(98)80012-2
26. Perera, M., Al-hebshi, N. N., Speicher, D. J., Perera, I., and Johnson, N. W. (2016). Emerging role of bacteria in oral carcinogenesis: a review with special reference to perio-pathogenic bacteria. J. Oral Microbiol. 8:32762. doi: 10.3402/jom.v8.32762
27. Pushalkar, S., Mane, S. P., Ji, X., Li, Y., Evans, C., Crasta, O. R., et al. (2011). Microbial diversity in saliva of oral squamous cell carcinoma. FEMS Immunol. Med. Microbiol. 61, 269-277. doi: 10.1111/j.1574-695X.2010.00773.x
28. Rubinstein, M. R., Wang, X., Liu, W., Hao, Y., Cai, G., and Han, Y. W. (2013). Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/b-catenin signaling via its FadA adhesin. Cell Host Microbe 14, 195-206. doi: 10.1016/j.chom.2013.07.012
29. Schloss, P. D. (2008). Evaluating different approaches that test whether microbial communities have the same structure. ISME J. 2, 265-275. doi: 10.1111/j.1365-294X.2007.03326.x
30. Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., et al. (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537-7541. doi: 10.1128/AEM.01541-09
31. Schmidt, B. L., Kuczynski, J., Bhattacharya, A., Huey, B., Corby, P. M., Queiroz, E. L. S., et al. (2014). Changes in abundance of oral microbiota associated with oral cancer. PLOS ONE 9:e98741. doi: 10.1371/journal.pone.0098741.s027
32. Scully, C., and Bagan, J. (2009). Oral squamous cell carcinoma: overview of current understanding of aetiopathogenesis and clinical implications. Oral Dis. 15, 388-399. doi: 10.1111/j.1601-0825.2009.01563.x
33. Segata, N., Izard, J., Waldron, L., Gevers, D., Miropolsky, L., Garrett, W. S., et al. (2011). Metagenomic biomarker discovery and explanation. Genome Biol. 12:R60. doi: 10.1186/gb-2011-12-6-r60
34. Silverman, S., Gorsky, M., and Lozada, F. (1984). Oral leukoplakia and malignant transformation. A follow-up study of 257 patients. Cancer 53, 563-568. doi: 10.1002/1097-0142(19840201)53:3<563::AID-CNCR2820530332>3.0.CO;2-F
35. Storey, J. D., and Tibshirani, R. (2003). Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. U.S.A. 100, 9440-9445. doi: 10.1073/pnas.1530509100
36. Warren, R. L., Freeman, D. J., Pleasance, S., Watson, P., Moore, R. A., Cochrane, K., et al. (2013). Co-occurrence of anaerobic bacteria in colorectal carcinomas. Microbiome 1:16. doi: 10.1186/2049-2618-1-16
37. White, J. R., Nagarajan, N., and Pop, M. (2009). Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLOS Comput. Biol. 5:e1000352. doi: 10.1371/journal.pcbi.1000352
38. Wu, J., Peters, B. A., Dominianni, C., Zhang, Y., Pei, Z., Yang, L., et al. (2016). Cigarette smoking and the oral microbiome in a large study of American adults. ISME J. 10, 2435-2446. doi: 10.1038/ismej.2016.37
39. Yamamura, K., Baba, Y., Nakagawa, S., Mima, K., Miyake, K., Nakamura, K., et al. (2016). Human microbiome Fusobacterium nucleatum in esophageal cancer tissue is associated with prognosis. Clin. Cancer Res. 22, 5574-5581. doi: 10.1158/1078-0432.CCR-16-1786
40. Yanik, E. L., Katki, H. A., Silverberg, M. J., Manos, M. M., Engels, E. A., and Chaturvedi, A. K. (2015). Leukoplakia, oral cavity cancer risk, and cancer survival in the U.S. elderly. Cancer Prev. Res. 8, 857-863. doi: 10.1158/1940-6207.CAPR-15-0091